Glucocorticoids antagonize tumor necrosis factor-α-stimulated lipolysis and resistance to the antilipolytic effect of insulin in human adipocytes

American Journal of Physiology - Endocrinology and Metabolism

Volumn 303, Issue 9, 2012, Pages

  Lee, Mi Jeong ^a   Fried, Susan K ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adipose triglyceride lipase; Dexamethasone; Hormone sensitive lipase; Obesity; Perilipin

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; DEXAMETHASONE; GLUCOCORTICOID; HORMONE SENSITIVE LIPASE; INSULIN; PERILIPIN; PHOSPHODIESTERASE III; PHOSPHODIESTERASE IIIB; SERINE; TRIACYLGLYCEROL LIPASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOSE TISSUE; ADULT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; INSULIN RESPONSE; INSULIN SENSITIVITY; LIPOLYSIS; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TISSUE CULTURE;

ADULT; CARRIER PROTEINS; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 3; DEXAMETHASONE; FEMALE; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; HUMANS; INSULIN; INSULIN RESISTANCE; LIPASE; LIPOLYSIS; MALE; MIDDLE AGED; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; STEROL ESTERASE; SUBCUTANEOUS FAT, ABDOMINAL; TISSUE CULTURE TECHNIQUES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84868330463     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00228.2012     Document Type: Article

References (46)

1. Beck IM, Vanden Berghe W, Vermeulen L, Yamamoto KR, Haegeman G, De Bosscher K. Crosstalk in inflammation: the interplay of glucocorticoid receptor-based mechanisms and kinases and phosphatases. Endocr Rev 30: 830-882, 2009.
2. Borst SE. The role of TNF-alpha in insulin resistance. Endocrine 23: 177-182, 2004.
3. Campbell JE, Peckett AJ, D'souza A, Hawke TJ, Riddell MC. Adipogenic and lipolytic effects of chronic glucocorticoid exposure. Am J Physiol Cell Physiol 300: C198-C209, 2011.
4. Cao YL, Hu CZ, Meng X, Wang DF, Zhang J. Expression of TNF-alpha protein in omental and subcutaneous adipose tissue in obesity. Diabetes Res Clin Pract 79: 214-219, 2008.
5. Cawthorn WP, Sethi JK. TNF-alpha and adipocyte biology. FEBS Lett 582: 117-131, 2008.
6. DeRijk R, Michelson D, Karp B, Petrides J, Galliven E, Deuster P, Paciotti G, Gold PW, Sternberg EM. Exercise and circadian rhythminduced variations in plasma cortisol differentially regulate interleukin-1 beta (IL-1 beta), IL-6, and tumor necrosis factor-alpha (TNF alpha) production in humans: high sensitivity of TNF alpha and resistance of IL-6. J Clin Endocrinol Metab 82: 2182-2191, 1997.
7. Divertie GD, Jensen MD, Miles JM. Stimulation of lipolysis in humans by physiological hypercortisolemia. Diabetes 40: 1228-1232, 1991.
8. Djurhuus CB, Gravholt CH, Nielsen S, Mengel A, Christiansen JS, Schmitz OE, Moller N. Effects of cortisol on lipolysis and regional interstitial glycerol levels in humans. Am J Physiol Endocrinol Metab 283: E172-E177, 2002.
9. Fried SK, Bunkin DA, Greenberg AS. Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid. J Clin Endocrinol Metab 83: 847-850, 1998.
10. Fried SK, Russell CD, Grauso NL, Brolin RE. Lipoprotein lipase regulation by insulin and glucocorticoid in subcutaneous and omental adipose tissues of obese women and men. J Clin Invest 92: 2191-2198, 1993.
11. Fried SK, Tittelbach T, Blumenthal J, Sreenivasan U, Robey L, Yi J, Khan S, Hollender C, Ryan AS, Goldberg AP. Resistance to the antilipolytic effect of insulin in adipocytes of African-American compared with Caucasian postmenopausal women. J Lipid Res 51: 1193-1200, 2010.
12. Gasic S, Tian B, Green A. Tumor necrosis factor alpha stimulates lipolysis in adipocytes by decreasing Gi protein concentrations. J Biol Chem 274: 6770-6775, 1999.
13. Hadri KE, Courtalon A, Gauthereau X, Chambaut-Guerin AM, Pairault J, Feve B. Differential regulation by tumor necrosis factor-alpha of beta1-, beta2-, and beta3-adrenoreceptor gene expression in 3T3-F442A adipocytes. J Biol Chem 272: 24514-24521, 1997.
14. Hauner H, Petruschke T, Russ M, Rohrig K, Eckel J. Effects of tumour necrosis factor alpha (TNF alpha) on glucose transport and lipid metabolism of newly-differentiated human fat cells in cell culture. Diabetologia 38: 764-771, 1995.
15. Hoppmann J, Perwitz N, Meier B, Fasshauer M, Hadaschik D, Lehnert H, Klein J. The balance between gluco-and mineralo-corticoid action critically determines inflammatory adipocyte responses. J Endocrinol 204: 153-164, 2010.
16. Lacasa D, Agli B, Giudicelli Y. Permissive action of glucocorticoids on catecholamine-induced lipolysis: direct "in vitro" effects on the fat cell beta-adrenoreceptor-coupled-adenylate cyclase system. Biochem Biophys Res Commun 153: 489-497, 1988.
17. Lamberts SW, Timmermans HA, Kramer-Blankestijn M, Birkenhager JC. The mechanism of the potentiating effect of glucocorticoids on catecholamine-induced lipolysis. Metabolism 24: 681-689, 1975.
18. Large V, Reynisdottir S, Langin D, Fredby K, Klannemark M, Holm C, Arner P. Decreased expression and function of adipocyte hormonesensitive lipase in subcutaneous fat cells of obese subjects. J Lipid Res 40: 2059-2066, 1999.
19. Laurencikiene J, van H, V, Arvidsson NE, Dicker A, Blomqvist L, Naslund E, Langin D, Arner P, Ryden M. NF-kappaB is important for TNF-alpha-induced lipolysis in human adipocytes. J Lipid Res 48: 1069-1077, 2007.
20. Lee MJ, Fried SK, Mundt SS, Wang Y, Sullivan S, Stefanni A, Daugherty BL, Hermanowski-Vosatka A. Depot-specific regulation of the conversion of cortisone to cortisol in human adipose tissue. Obesity (Silver Spring) 16: 1178-1185, 2008.
21. Lee MJ, Gong DW, Burkey BF, Fried SK. Pathways regulated by glucocorticoids in omental and subcutaneous human adipose tissues: a microarray study. Am J Physiol Endocrinol Metab 300: E571-E580, 2011.
22. Lee MJ, Wu Y, Fried SK. A modified protocol to maximize differentiation of human preadipocytes and improve metabolic phenotypes. Obesity (Silver Spring) 2012 May 4. doi:10.1038/oby.2012.116. [Epub ahead of print].
23. Lundgren M, Buren J, Lindgren P, Myrnas T, Ruge T, Eriksson JW. Sex-and depot-specific lipolysis regulation in human adipocytes: interplay between adrenergic stimulation and glucocorticoids. Horm Metab Res 40: 854-860, 2008.
24. Ottosson M, Lonnroth P, Bjorntorp P, Eden S. Effects of cortisol and growth hormone on lipolysis in human adipose tissue. J Clin Endocrinol Metab 85: 799-803, 2000.
25. Patsouris D, Neels JG, Fan W, Li PP, Nguyen MT, Olefsky JM. Glucocorticoids and thiazolidinediones interfere with adipocyte-mediated macrophage chemotaxis and recruitment. J Biol Chem 284: 31223-31235, 2009.
26. Peckett AJ, Wright DC, Riddell MC. The effects of glucocorticoids on adipose tissue lipid metabolism. Metabolism 60: 1500-1510, 2011.
27. Petrovsky N, McNair P, Harrison LC. Diurnal rhythms of pro-inflammatory cytokines: regulation by plasma cortisol and therapeutic implications. Cytokine 10: 307-312, 1998.
28. Porter MH, Cutchins A, Fine JB, Bai Y, DiGirolamo M. Effects of TNF-alpha on glucose metabolism and lipolysis in adipose tissue and isolated fat-cell preparations. J Lab Clin Med 139: 140-146, 2002.
29. Rahn LT, Mei J, Karlsson M, Manganiello V, Degerman E. Downregulation of cyclic-nucleotide phosphodiesterase 3B in 3T3-L1 adipocytes induced by tumour necrosis factor alpha and cAMP. Biochem J 346: 337-343, 2000.
30. Ranjit S, Boutet E, Gandhi P, Prot M, Tamori Y, Chawla A, Greenberg AS, Puri V, Czech MP. Regulation of fat specific protein 27 by isoproterenol and TNF-alpha to control lipolysis in murine adipocytes. J Lipid Res 52: 221-236, 2011.
31. Rask E, Olsson T, Soderberg S, Andrew R, Livingstone DE, Johnson O, Walker BR. Tissue-specific dysregulation of cortisol metabolism in human obesity. J Clin Endocrinol Metab 86: 1418-1421, 2001.
32. Ros M, Northup JK, Malbon CC. Adipocyte G-proteins and adenylate cyclase. Effects of adrenalectomy. Biochem J 257: 737-744, 1989.
33. Rosenstock M, Greenberg AS, Rudich A. Distinct long-term regulation of glycerol and non-esterified fatty acid release by insulin and TNF-alpha in 3T3-L1 adipocytes. Diabetologia 44: 55-62, 2001.
34. Russell CD, Petersen RN, Rao SP, Ricci MR, Prasad A, Zhang Y, Brolin RE, Fried SK. Leptin expression in adipose tissue from obese humans: depot-specific regulation by insulin and dexamethasone. Am J Physiol Endocrinol Metab 275: E507-E515, 1998.
35. Samra JS, Clark ML, Humphreys SM, Macdonald IA, Bannister PA, Frayn KN. Effects of physiological hypercortisolemia on the regulation of lipolysis in subcutaneous adipose tissue. J Clin Endocrinol Metab 83: 626-631, 1998.
36. Samra JS, Clark ML, Humphreys SM, Macdonald IA, Matthews DR, Frayn KN. Effects of morning rise in cortisol concentration on regulation of lipolysis in subcutaneous adipose tissue. Am J Physiol Endocrinol Metab 271: E996-E1002, 1996.
37. Sandeep TC, Andrew R, Homer NZ, Andrews RC, Smith K, Walker BR. Increased in vivo regeneration of cortisol in adipose tissue in human obesity and effects of the 11beta-hydroxysteroid dehydrogenase type 1 inhibitor carbenoxolone. Diabetes 54: 872-879, 2005.
38. Shen WJ, Patel S, Natu V, Kraemer FB. Mutational analysis of structural features of rat hormone-sensitive lipase. Biochemistry 37: 8973-8979, 1998.
39. Souza SC, Palmer HJ, Kang YH, Yamamoto MT, Muliro KV, Paulson KE, Greenberg AS. TNF-alpha induction of lipolysis is mediated through activation of the extracellular signal related kinase pathway in 3T3-L1 adipocytes. J Cell Biochem 89: 1077-1086, 2003.
40. Tansey JT, Sztalryd C, Hlavin EM, Kimmel AR, Londos C. The central role of perilipin a in lipid metabolism and adipocyte lipolysis. IUBMB Life 56: 379-385, 2004.
41. Trujillo ME, Sullivan S, Harten I, Schneider SH, Greenberg AS, Fried SK. Interleukin-6 regulates human adipose tissue lipid metabolism and leptin production in vitro. J Clin Endocrinol Metab 89: 5577-5582, 2004.
42. van Raalte DH, Brands M, van der Zijl NJ, Muskiet MH, Pouwels PJ, Ackermans MT, Sauerwein HP, Serlie MJ, Diamant M. Low-dose glucocorticoid treatment affects multiple aspects of intermediary metabolism in healthy humans: a randomised controlled trial. Diabetologia 54: 2103-2112, 2011.
43. Xu C, He J, Jiang H, Zu L, Zhai W, Pu S, Xu G. Direct effect of glucocorticoids on lipolysis in adipocytes. Mol Endocrinol 2009.
44. Yu CY, Mayba O, Lee JV, Tran J, Harris C, Speed TP, Wang JC. Genome-wide analysis of glucocorticoid receptor binding regions in adipocytes reveal gene network involved in triglyceride homeostasis. PLoS One 5: e15188, 2010.
45. Zhang HH, Halbleib M, Ahmad F, Manganiello VC, Greenberg AS. Tumor necrosis factor-alpha stimulates lipolysis in differentiated human adipocytes through activation of extracellular signal-related kinase and elevation of intracellular cAMP. Diabetes 51: 2929-2935, 2002.
46. Zimmermann R, Lass A, Haemmerle G, Zechner R. Fate of fat: the role of adipose triglyceride lipase in lipolysis. Biochim Biophys Acta 1791: 494-500, 2009.